The Relationship Between Serial [18 F]PBR06 PET Imaging of Microglial Activation and Motor Function Following Stroke in Mice

Molecular Imaging and Biology

Volumn 16, Issue 6, 2014, Pages 821-829

  Lartey, Frederick M ^a   Ahn, G One ^c   Ali, Rehan ^a   Rosenblum, Sahar ^a   Miao, Zheng ^a   Arksey, Natasha ^a   Shen, Bin ^a   Colomer, Marta Vilalta ^a   Rafat, Marjan ^a   Liu, Hongguang ^a   Alejandre Alcazar, Miguel A ^a   Chen, John W ^d   Palmer, Theo ^a   Chin, Frederick T ^a   Guzman, Raphael ^a,e   Loo, Billy W ^a,b   Graves, Edward ^a,b  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD CANCER INSTITUTE   (United States)

^c Pohang University of Science and Technology (POSTECH)   (South Korea)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Mice; Microglia; Minocycline; Motor function; Neuroinflammation; Stroke; 18 F PBR06 PET imaging

Indexed keywords

MINOCYCLINE; PBR 06 F 18; RADIOLIGAND; UNCLASSIFIED DRUG; ACETANILIDE DERIVATIVE; CONTRAST MEDIUM; FLUORINE; N-FLUOROACETYL-N-(2,5-DIMETHOXYBENZYL)-2-PHENOXYANILINE; RADIOPHARMACEUTICAL AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CEREBROVASCULAR ACCIDENT; CLINICAL ASSESSMENT TOOL; COMPUTER ASSISTED EMISSION TOMOGRAPHY; CONTROLLED STUDY; DISEASE COURSE; FEMALE; IMMUNOHISTOCHEMISTRY; MICROGLIA; MIDDLE CEREBRAL ARTERY OCCLUSION; MOTOR PERFORMANCE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR MAGNETIC RESONANCE SCANNER; PET-CT SCANNER; POSITRON EMISSION TOMOGRAPHY; PROTEIN EXPRESSION; ROTAROD TEST; ANIMAL; BAGG ALBINO MOUSE; MOTOR ACTIVITY; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; SCINTISCANNING;

MUS;

ACETANILIDES; ANIMALS; CONTRAST MEDIA; FEMALE; FLUORINE RADIOISOTOPES; MICE; MICE, INBRED BALB C; MICROGLIA; MINOCYCLINE; MOTOR ACTIVITY; POSITRON-EMISSION TOMOGRAPHY; RADIOPHARMACEUTICALS; STROKE;

EID: 84911967385     PISSN: 15361632     EISSN: 18602002     Source Type: Journal    
DOI: 10.1007/s11307-014-0745-0     Document Type: Article

References (40)

1. Coull BM (2007) Inflammation and stroke—introduction. Stroke 38:631
2. Wang Q, Tang XN, Yenari MA (2007) The inflammatory response in stroke. J Neuroimmunol 184:53–68
3. Milner R (2009) Microglial expression of alphavbeta3 and alphavbeta5 integrins is regulated by cytokines and the extracellular matrix: beta5 integrin null microglia show no defects in adhesion or MMP-9 expression on vitronectin. Glia 57:714–723
4. Crack PJ, Taylor JM (2005) Reactive oxygen species and the modulation of stroke. Free Radic Biol Med 38:1433–1444
5. Liu Z, Fan Y, Won SJ et al (2007) Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38:146–152
6. Barreto G, Huang TT, Giffard RG (2010) Age-related defects in sensorimotor activity, spatial learning, and memory in C57BL/6 mice. J Neurosurg Anesthesiol 22:214–219
7. Palmer TD, Monje ML, Toda H (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760–1765
8. Tatemichi TK, Desmond DW, Stern Y et al (1994) Cognitive impairment after stroke: frequency, patterns, and relationship to functional abilities. J Neurol Neurosurg Psychiatry 57:202–207
9. Papadopoulos V, Baraldi M, Guilarte TR et al (2006) Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27:402–409
10. James ML, Fulton RR, Vercoullie J et al (2008) DPA-714, a new translocator protein-specific ligand: synthesis, radiofluorination, and pharmacologic characterization. J Nucl Med 49:814–822
11. Gerhard A, Neumaier B, Elitok E et al (2000) In vivo imaging of activated microglia using [11C]PK11195 and positron emission tomography in patients after ischemic stroke. Neuroreport 11:2957–2960
12. Cagnin A, Kassiou M, Meikle SR, Banati RB (2007) Positron emission tomography imaging of neuroinflammation. Neurotherapeutics 4:443–452
13. Imaizumi M, Kim HJ, Zoghbi SS et al (2007) PET imaging with [11C]PBR28 can localize and quantify upregulated peripheral benzodiazepine receptors associated with cerebral ischemia in rat. Neurosci Lett 411:200–205
14. James ML, Fulton RR, Henderson DJ et al (2005) Synthesis and in vivo evaluation of a novel peripheral benzodiazepine receptor PET radioligand. Bioorg Med Chem 13:6188–6194
15. Yui J, Hatori A, Kawamura K et al (2011) Visualization of early infarction in rat brain after ischemia using a translocator protein (18 kDa) PET ligand [11C]DAC with ultra-high specific activity. Neuroimage 54:123–130
16. Yui J, Maeda J, Kumata K et al (2010) 18 F-FEAC and 18 F-FEDAC: PET of the monkey brain and imaging of translocator protein (18 kDa) in the infarcted rat brain. J Nucl Med 51:1301–1309
17. Lartey FM, Ahn GO, Shen B et al (2014) PET imaging of stroke-induced neuroinflammation in mice using [F]PBR06. Mol Imaging Biol 16(1):109–117
18. Martin A, Boisgard R, Kassiou M, Dolle F, Tavitian B (2011) Reduced PBR/TSPO expression after minocycline treatment in a rat model of focal cerebral ischemia: a pet study using [F-18]DPA-714. Mol Imaging Biol 13:10–15
19. Liu ZY, Fan Y, Won SJ et al (2007) Chronic treatment with minocycline preserves adult new neurons and reduces functional impairment after focal cerebral ischemia. Stroke 38:146–152
20. Briard E, Zoghbi SS, Simeon FG et al (2009) Single-step high-yield radiosynthesis and evaluation of a sensitive 18 F-labeled ligand for imaging brain peripheral benzodiazepine receptors with PET. J Med Chem 52:688–699
21. Mao Y, Yang GY, Zhou LF, Stern JD, Betz AL (1999) Focal cerebral ischemia in the mouse: description of a model and effects of permanent and temporary occlusion. Brain Res Mol Brain Res 63:366–370
22. Sakata H, Niizuma K, Yoshioka H et al (2012) Minocycline-preconditioned neural stem cells enhance neuroprotection after ischemic stroke in rats. J Neurosci 32:3462–3473
23. Lartey FM, Ahn GO, Shen B et al (2014) PET imaging of stroke-induced neuroinflammation in mice using [(18)F]PBR06. Mol Imaging Biol: MIB: Off Publ Acad Mol Imaging 16:109–117
24. Hudson HM, Larkin RS (1994) Accelerated image reconstruction using ordered subsets of projection data. IEEE Trans Med Imaging 13:601–609
25. Habte F, Ren G, Doyle TC et al (2013) Impact of a multiple mice holder on quantitation of high-throughput micropet imaging with and without Ct attenuation correction. Mol Imaging Biol 15:569–575
26. Graves EE, Quon A, Loo BW Jr (2007) RT_Image: an open-source tool for investigating PET in radiation oncology. Technol Cancer Res Treat 6:111–121
27. Yui J, Hatori A, Kawamura K et al (2011) Visualization of early infarction in rat brain after ischemia using a translocator protein (18 kDa) PET ligand [C-11]DAC with ultra-high specific activity. Neuroimage 54:123–130
28. Carson MJ, Bilousova TV, Puntambekar SS et al (2007) A rose by any other name? The potential consequences of microglial heterogeneity during CNS health and disease. Neurotherapeutics 4:571–579
29. Martin A, Boisgard R, Theze B et al (2010) Evaluation of the PBR/TSPO radioligand [F-18]DPA-714 in a rat model of focal cerebral ischemia. J Cereb Blood Flow Metab 30:230–241
30. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91:461–553
31. Chen MK, Guilarte TR (2008) Translocator protein 18 kDa (TSPO): molecular sensor of brain injury and repair. Pharmacol Ther 118:1–17
32. Perego C, De Fumagalli S, Simoni MG (2011) Temporal pattern of expression and colocalization of microglia/macrophage phenotype markers following brain ischemic injury in mice. J Neuroinflammation 8:174. doi:10.1186/1742B2094B8B174
33. Martin A, Boisgard R, Theze B et al (2010) Evaluation of the PBR/TSPO radioligand [(18)F]DPA-714 in a rat model of focal cerebral ischemia. J Cereb Blood Flow Metab 30:230–241
34. Breckwoldt MO, Chen JW, Stangenberg L et al (2008) Tracking the inflammatory response in stroke in vivo by sensing the enzyme myeloperoxidase. Proc Natl Acad Sci U S A 105:18584–18589
35. d'Avila JC, Lam TI, Bingham D et al (2012) Microglial activation induced by brain trauma is suppressed by post-injury treatment with a PARP inhibitor. J Neuroinflammation 9:31
36. Rupalla K, Allegrini PR, Sauer D, Wiessner C (1998) Time course of microglia activation and apoptosis in various brain regions after permanent focal cerebral ischemia in mice. Acta Neuropathol 96:172–178
37. Zhang ZG, Zhang L, Jiang Q et al (2000) VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest 106:829–838
38. Rueger MA, Muesken S, Walberer M et al (2012) Effects of minocycline on endogenous neural stem cells after experimental stroke. Neuroscience 215:174–183
39. Hayakawa K, Mishima K, Nozako M et al (2008) Delayed treatment with minocycline ameliorates neurologic impairment through activated microglia expressing a high-mobility group box1-inhibiting mechanism. Stroke 39:951–958
40. Converse AK, Larsen EC, Engle JW et al (2011) C-11-(R)-PK11195 PET imaging of microglial activation and response to minocycline in Zymosan-treated rats. J Nucl Med 52:257–262